Increase of Excavating Sponges on Caribbean Coral Reefs: Reproduction, Dispersal, and Coral Deterioration

Coral reefs ecosystems are deteriorating and facing dramatic changes. These changes suggest a shift in dominance from corals to other benthic organisms. Particularly in the Caribbean Sea, with corals dying, sponges have become the leading habitat-forming benthic animals. However, little is known about what life-history traits allow organisms to proliferate in a marine system that is undergoing change. Thus, the objective of this dissertation was to try to understand the current increase of encrusting excavating sponges on deteriorating Caribbean coral reefs through the study of reproduction, recruitment and dispersal potential of the widely distributed and currently expanding species, Cliona delitrix. Different methodological approaches were used, such as histology, electron microscopy, quantification of sponges in the field, genetics, and mathematical modeling. Results are presented in four different chapters. It was found that Cliona delitrix has an extended reproductive cycle in Florida, USA, from April - May to around November - December depending on a \u3e25°C sea-water temperature threshold. C. delitrix gametogenesis is asynchronous and it has multiple spawning events. C. delitrix is recruiting abundantly on Caribbean coral reefs, preferentially on recent coral mortality than on old coral mortality. The increase in C. delitrix and other excavating sponges can be explained by the repeated spawning and by the coincidence in time and space of larval production with the availability of new dead coral, which tend to overlap during the warmest months of the year. Eggs or larvae of C. delitrix appear to survive enough to be transported by currents over larger distances. It was found that dispersal ranges for Cliona delitrix may reach as far as ~315 km in the Florida reef track, and over ~971 km in the South Caribbean Sea, between Belize and Panama. Thus, reproduction, dispersal, and recruitment patterns of C. delitrix along with oceanographic currents, and eddies that form at different periods of time, are sustaining the spread of this sponge on coral reefs. According to mathematical models carried out, C. delitrix increase on reefs fluctuates depending of coral mortality events and available space on old dead coral (colonized by algae and other invertebrates). However, under temperature anomalies, these sponges will 2 tend to increase and take over the reef system only if heat stress and coral mortality is moderate. Under massive mortality events both corals and sponges will tend to decline, although sponges at a slower rate than corals. In general, coral excavating sponges have been favored by coral mortality, especially during past few decades. However as bioeroders, their success is also limited by the success of calcifying corals. In a reef management context and based on this dissertation’s findings, it is suggested that excavating sponges, and especially Cliona delitrix, should be more formally included in reef monitoring programs. Their increase can be used to track coral mortality events on reefs (past and future), and also can be used as another major bioindicator of health on coral reefs

Coral-Excavating Sponge Cliona delitrix: Current Trends of Space Occupation on High Latitude Coral Reefs

The recent increase in abundance of coral-excavating sponges is a threat to the health of coral reefs. However, the distribution and growth of these sponges are poorly documented on high latitude reefs where corals live in marginal environmental conditions. In this study, we characterize the current trends of space occupation of Cliona delitrix on high latitude reefs (26°N) in southeast Florida. C. delitrix densities were significantly higher on the deepest habitat of this reef tract (the outer reef) in response to a higher availability of coral substratum. Sponge growth rates increased with depth, and in relation to presence of tunicates and absence of macroalgae living in the sponge–coral interaction band. Conversely, coral tissue loss was similar between habitats, regardless of the fouling organisms present in the band between sponge and coral. On high latitude reefs, C. delitrix preferred massive scleractinian coral species as substratum, similar to tropical reefs, but its inclination for specific coral species varied. The outer reef sites (deepest habitat) are most vulnerable to C. delitrix colonization. Reef habitats with higher coral densities and more available dead coral may continue to suffer the greatest levels of sponge bioerosion

Population Structure and Dispersal of the Coral-Excavating Sponge Cliona delitrix

Some excavating sponges of the genus Cliona compete with live reef corals, often killing and bioeroding entire colonies. Important aspects affecting distribution of these species, such as dispersal capability and population structure, remain largely unknown. Thus, the aim of this study was to determine levels of genetic connectivity and dispersal of Cliona delitrix across the Greater Caribbean (Caribbean Sea, Bahamas and Florida), to understand current patterns and possible future trends in their distribution and effects on coral reefs. Using ten species-specific microsatellite markers, we found high levels of genetic differentiation between six genetically distinct populations: one in the Atlantic (Florida-Bahamas), one specific to Florida and four in the South Caribbean Sea. In Florida, two independent breeding populations are likely separated by depth. Gene flow and ecological dispersal occur among other populations in the Florida reef tract, and between some Florida locations and the Bahamas. Similarly, gene flow occurs between populations in the South Caribbean Sea, but appears restricted between the Caribbean Sea and the Atlantic (Florida-Bahamas). Dispersal of C. delitrix was farther than expected for a marine sponge and favoured in areas where currents are strong enough to transport sponge eggs or larvae over longer distances. Our results support the influence of ocean current patterns on genetic connectivity, and constitute a baseline to monitor future C. delitrix trends under climate change

Coral recruitment is impacted by the presence of a sponge community

© 2019 Peng Luo et al., published by De Gruyter, Berlin/Boston. C23H13NO4, monoclinic, P21/n (no. 14), a = 11.6537(6) Å, b = 5.1315(2) Å, c = 26.8047(13) Å, β = 96.266(3)°, V = 1593.4(13) Å3, Z = 4, Rgt(F) = 0.0531, wRref(F2) = 0.1432, T = 90.0(5) K

Siderastrea siderea Spawning and Oocyte Resorption at High Latitude

At high latitudes (\u3e25°), sexual reproduction and the maintenance of coral populations can be impaired by marginal environmental conditions. However, little is known about sexual reproduction of many coral species at high latitude on the northern-most extension of the Florida Reef Tract. This study aimed to histologically characterize the reproductive ecology of Siderastrea siderea, near Fort Lauderdale, Florida (26°N). Tissue samples of S. siderea were collected semi-monthly to multiweekly from August to November in 2007 and 2008. Spawning was inferred from gametogenesis and oocyte resorption was observed in detail. Environmental variables including temperature and lunar cycle were examined for relationship with potential spawning times. Based on the histological evidence, we infer that spawning likely occurred primarily in October. Gametogenesis in this species is likely mediated by seasonal temperature variation, whereas lunar cycle could act as finer scale environmental cue for coordination of spawning. Our findings highlight that S. siderea spawning occurs later in the year compared to other populations of this species throughout the Caribbean and to other coral species near Fort Lauderdale. For the first time, oocyte resorption stages are described and constitute a baseline for future projects that aim to understand this process in corals

Fecundity and Sexual Maturity of the Coral Siderastrea siderea at High Latitude Along the Florida Reef Tract, USA

Siderastrea siderea is one of the most abundant corals at high latitude shallow sites along the Florida Reef Tract (25°–27°N). This species is able to tolerate wide seawater temperature fluctuations and sedimentation stress, but its reproductive status at high latitudes and under marginal environmental conditions is poorly understood. The objectives of this study were to evaluate the reproductive potential of S. siderea along a latitudinal gradient (25°–27°N) and to determine if sexual maturity occurs in small (\u3c12.0 cm) S. siderea colonies. Samples of coral tissue were collected in 2007, 2008, and 2009 at three sites along the latitudinal gradient and were processed for histological analysis. Oocyte size, volume, and abundance were used to calculate fecundity. Results showed that fecundity decreased with increasing latitude and that oocyte volume was the major contributing factor to this variation. Mature oocytes were observed in S. siderea colonies at sizes as small as 1.1 cm in diameter. The ability of S. siderea to reach fertility at high latitude areas suggests this species is able to reproduce under marginal environmental conditions; however, reduction in oocyte size could increase local retention of larvae. The presence of mature oocytes in small colonies suggests that stress can reduce somatic growth and shift sexual maturity to smaller colony sizes

Reconstruction of Family-Level Phylogenetic Relationships within Demospongiae (Porifera) Using Nuclear Encoded Housekeeping Genes

Background: Demosponges are challenging for phylogenetic systematics because of their plastic and relatively simple morphologies and many deep divergences between major clades. To improve understanding of the phylogenetic relationships within Demospongiae, we sequenced and analyzed seven nuclear housekeeping genes involved in a variety of cellular functions from a diverse group of sponges. Methodology/Principal Findings: We generated data from each of the four sponge classes (i.e., Calcarea, Demospongiae, Hexactinellida, and Homoscleromorpha), but focused on family-level relationships within demosponges. With data for 21 newly sampled families, our Maximum Likelihood and Bayesian-based approaches recovered previously phylogenetically defined taxa: Keratosap, Myxospongiaep, Spongillidap, Haploscleromorphap (the marine haplosclerids) and Democlaviap. We found conflicting results concerning the relationships of Keratosap and Myxospongiaep to the remaining demosponges, but our results strongly supported a clade of Haploscleromorphap+Spongillidap+Democlaviap. In contrast to hypotheses based on mitochondrial genome and ribosomal data, nuclear housekeeping gene data suggested that freshwater sponges (Spongillidap) are sister to Haploscleromorphap rather than part of Democlaviap. Within Keratosap, we found equivocal results as to the monophyly of Dictyoceratida. Within Myxospongiaep, Chondrosida and Verongida were monophyletic. A well supported clade within Democlaviap, Tetractinellidap, composed of all sampled members of Astrophorina and Spirophorina (including the only lithistid in our analysis), was consistently revealed as the sister group to all other members of Democlaviap. Within Tetractinellidap, we did not recover monophyletic Astrophorina or Spirophorina. Our results also reaffirmed the monophyly of order Poecilosclerida (excluding Desmacellidae and Raspailiidae), and polyphyly of Hadromerida and Halichondrida. Conclusions/Significance: These results, using an independent nuclear gene set, confirmed many hypotheses based on ribosomal and/or mitochondrial genes, and they also identified clades with low statistical support or clades that conflicted with traditional morphological classification. Our results will serve as a basis for future exploration of these outstanding questions using more taxon- and gene-rich datasets

Effects of Excavating-Sponge Removal on Coral Growth

Some excavating sponges are strong competitors for space on coral reefs, able to kill live coral tissue and to overgrow entire coral colonies. Stony corals with excavating sponges can die or become dislodged. To date no restoration efforts to eliminate excavating sponges from live corals have been considered. In this study we examined the effect and remedial potential of removal of the excavating sponge, Cliona delitrix, by monitoring tissue loss of the stony coral Montastrea cavernosa. Thirty-three corals colonized by the sponge were used: 11 as controls, and 22 as treatments in which sponges were removed using hammer and chisel. After sponge removal, resultant cavities in the coral skeletons were filled with common cement or epoxy. Standardized photos of each coral were taken immediately after sponge removal, and at 6 and 12 months afterwards. Results were similar between fill materials and showed a reduction in coral tissue loss in colonies where the sponge was removed. This study demonstrates that eliminating the bioeroding sponge enables potential recovery in affected stony corals after a year. However, 36% of experimental corals showed renewed presence of C. delitrix on the colony surface within a year after removal, demonstrating the extraordinary ability of this sponge to colonize corals. Although the technique used in this study is applicable to enhance modern coral restoration practices by slowing tissue loss, this method is costly, elaborate, and not suitable at a reef-wide scale. Further restoration alternatives and long-term measures to prevent over-colonization of corals by excavating sponges are encouraged

Asynchronous Reproduction and Multi-Spawning in the Coral-Excavating Sponge Cliona delitrix

Cliona delitrix is one of the most abundant and destructive coral-excavating sponges on Caribbean reefs. However, basic aspects of its reproductive biology, which largely determine the species propagation potential, remain unknown. A 2-year study (October 2009 to September 2011) was conducted to determine the reproductive cycle and gametogenesis of a C. delitrix population located in a shallow reef in Florida, USA. Mesohyl tissue collected from randomly chosen and tagged sponge individuals was sampled one to several times a month, and analysed by light and transmission electron microscopy (TEM). Cliona delitrix is oviparous and gonochoric, except for a few simultaneous hermaphroditic individuals. The C. delitrix reproductive cycle in Florida is from April to December, and is triggered by an increase in seawater temperature to 25°C. Oogenesis and spermatogenesis were asynchronous among individuals; with different cohorts of oocytes co-occurring in females, and spermatic cysts in males. Granulose cells acted as nurse cells, contributing to the growth and maturation of both female and male gametes. Spawning of gametes was not always synchronized with full moon phase. Unlike most other oviparous sponges, the reproductive cycle of C. delitrixis versatile and includes multiple spawning events during the summer of each year. This characteristic maximizes sponge propagation on coral reefs during the warmer months of the year, particularly when thermal stress induces coral mortality. This aspect, combined with its success on polluted areas, make C. delitrix a suitable bioindicator of coral reef health